Fungal Communities in Hydrocarbon Degradation

  • Francesc X. Prenafeta-BoldúEmail author
  • G. Sybren de Hoog
  • Richard C. Summerbell
Reference work entry
Part of the Handbook of Hydrocarbon and Lipid Microbiology book series (HHLM)


The present chapter reviews and discusses recent advances in the ecophysiology, phylogeny, and biotechnological applications of fungi with respect to their ability to degrade hydrocarbons. There is a very wide fungal biodiversity with diverse enzymatic mechanisms that transform different hydrocarbon chemical structures, from short chain aliphatics to heavy weight polycyclic aromatics. Alkanes and alkylbenzenes are generally metabolized as the sole source of carbon and energy via specialized metabolic pathways that start with the substrate oxidation through cytochrome P450 monoxygenases. Unsaturated alkenes and alkynes, as well as alicyclics, are more recalcitrant to fungal degradation and are often converted to partly oxidized metabolites. Aromatic hydrocarbons ranging from the single benzene ring to the high-molecular-weight polycyclics are generally degraded via one or more of three independent enzymatic systems. The intracellular P450 monooxygenases that detoxify harmful chemicals are universally present in the microsomes of eukaryotic cells, while lignin-degrading fungi specifically produce extracellular peroxidases and laccases that biodegrade aromatic hydrocarbons. Laccases are not exclusively active in lignin biodegradation: other functions have been reported for these enzymes in nonligninolytic fungi. The low functional specificity and high redox potential of peroxidases and laccases enables the oxidation of a broad range of aromatic hydrocarbons and other recalcitrant contaminants. Such co-incidental biodegradation processes often result in partially degraded compounds that do not support fungal growth and that might be more toxic than the parent substrates.

Relevant hydrocarbonoclastic fungal strains deposited in culture collections have been identified and their phylogenies revised and reassessed when necessary. The capacity to assimilate hydrocarbons in fungi may have evolved in the context of biotrophic interactions in environments that are rich in naturally biosynthesized alkanes and volatile alkylbenzenes. The ability to utilize hydrocarbons seems to correlate with virulence toward humans, as seen in phylogenetically unrelated genera of hydrocarbonoclastic fungi, e.g., Scedosporium (Microascales) and Exophiala-Cladophialophora (Chaetothyriales). Applied research on hydrocarbonoclastic fungi includes studies dedicated to preventing biodeterioration as well as on potential use of the same enzymatic capabilities for bioremediation purposes. Fungal contamination of fuels is a long-standing problem that has acquired new dimensions as new biofuel blends have emerged. Recent improvements in phylogenetic understanding of fungal biodeteriogens may provide enhanced biocontrol opportunities. In work related to restoration of ecosystems, the ability of hydrocarbonoclastic fungi to form extended mycelial networks, in combination with the broad capabilities of their catabolic enzymes, makes these fungi well suited for the bioremediation of hydrocarbon-polluted soils. However, some cases of unsatisfactory biodegradation efficiency in operations conducted at field scale and cases in which toxic intermediates were generated have turned research efforts towards synergistic biodegradation processes mediated by complex microbial populations (i.e., fungal-bacterial mixtures). The assimilatory biodegradation of volatile alkanes and alkylbenzenes by certain fungal species makes them ideal candidates for the biofiltration of air polluted with these compounds. However, the potential correlation between hydrocarbon utilization and capacity for human infection must be taken into account in the design of biofiltration systems in order to prevent unintended production of biohazardous conditions. Ongoing research is focusing on the precise delimitation of genetic mechanisms that underlie these two apparently converging ecological traits.



This research was supported by the CERCA Programme/Generalitat de Catalunya and by the IRTA Seed Research Fund Program. Francesc Prenafeta-Boldú is the coordinator of the Consolidated Research Group TERRA, funded by the Generalitat de Catalunya (2017 SGR 1290). We are thankful to Leandro Moreno for the critical reading of the manuscript. The collaboration of Daniela Isola, Derlene Attili de Angelis, and Fernando Carlos Pagnocca in providing graphical material is also acknowledged.


  1. Amin H, Atkins PT, Russo RS, Brown AW, Sive B, Hallar AG, Huff Hartz KE (2012) Effect of bark beetle infestation on secondary organic aerosol precursor emissions. Environ Sci Technol 46(11):5696–5703PubMedCrossRefGoogle Scholar
  2. Andersson BE, Lundstedt S, Tornberg K, Schnürer Y, Öberg LG, Mattiasson B (2003) Incomplete degradation of polycyclic aromatic hydrocarbons in soil inoculated with wood-rotting fungi and their effect on the indigenous soil bacteria. Environm Toxicol Chem 22(6):1238–1243CrossRefGoogle Scholar
  3. April TM, Abbott SP, Foght JM, Currah RS (1998) Degradation of hydrocarbons in crude oil by the ascomycete Pseudallescheria boydii (Microascaceae). Can J Microbiol 44(3):270–278PubMedCrossRefGoogle Scholar
  4. Aranda E, Marco-Urrea E, Caminal G, Arias ME, García-Romera I, Guillén F (2010) Advanced oxidation of benzene, toluene, ethylbenzene and xylene isomers (BTEX) by Trametes versicolor. J Hazard Mater 181(1):181–186PubMedCrossRefGoogle Scholar
  5. Arriaga S, Revah S (2005) Improving hexane removal by enhancing fungal development in a microbial consortium biofilter. Biotechnol Bioeng 90(1):107–115PubMedCrossRefGoogle Scholar
  6. Asha S, Vidyavathi M (2009) Cunninghamella – a microbial model for drug metabolism studies – a review. Biotechnol Adv 27(1):16–29PubMedCrossRefGoogle Scholar
  7. Badali H, Gueidan C, Najafzadeh MJ, Bonifaz A, van den Ende AHGG, de Hoog GS (2008) Biodiversity of the genus Cladophialophora. Stud Mycol 61(1):175–191PubMedPubMedCentralCrossRefGoogle Scholar
  8. Badali H, Carvalho VO, Vicente VA, Attili-Angelis D, Kwiatkowski IB, Van den Ende AHG, de Hoog GS (2009) Cladophialophora saturnica sp. nov., a new opportunistic species of Chaetothyriales revealed using molecular data. Med Mycol 47(1):51–62PubMedCrossRefGoogle Scholar
  9. Badali H, Prenafeta-Boldú FX, Guarro J, Klaassen C, Meis JF, de Hoog GS (2011) Cladophialophora psammophila, a novel species of Chaetothyriales with a potential use in the bioremediation of volatile aromatic hydrocarbons. Fungal Biol 115(10):1019–1029PubMedCrossRefGoogle Scholar
  10. Baldrian P (2006) Fungal laccases – occurrence and properties. FEMS Microbiol Rev 30(2):215–242PubMedCrossRefGoogle Scholar
  11. Banitz T, Johst K, Wick LY, Schamfuß S, Harms H, Frank K (2013) Highways versus pipelines: contributions of two fungal transport mechanisms to efficient bioremediation. Environ Microbiol Rep 5(2):211–218PubMedCrossRefGoogle Scholar
  12. Barth G, Gaillardin C (1996) Nonconventional yeasts in biotechnology: a handbook. Springer, Berlin/Heidelberg, pp 313–388CrossRefGoogle Scholar
  13. Beopoulos A, Desfougeres T, Sabirova J, Zinjarde S, Neuvéglise C, Nicaud J-M (2010) In: Timmis KN (ed) Handbook of hydrocarbon and lipid microbiology. Springer, Berlin/Heidelberg, pp 2111–2121CrossRefGoogle Scholar
  14. Blasi B, Poyntner C, Rudavsky T, Prenafeta-Boldú FX, Hoog SD, Tafer H, Sterflinger K (2016) Pathogenic yet environmentally friendly? Black fungal candidates for bioremediation of pollutants. Geomicrobiol J 33(3–4):308–317PubMedPubMedCentralCrossRefGoogle Scholar
  15. Blasi B, Tafer H, Kustor C, Poyntner C, Lopandic K, Sterflinger K (2017) Genomic and transcriptomic analysis of the toluene degrading black yeast Cladophialophora immunda. Sci Rep 7(1):11436PubMedPubMedCentralCrossRefGoogle Scholar
  16. Boulton C, Ratledge C (1984) Physiology of hydrocarbon-utilizing microorganisms. Top Enzym Ferment Biotechnol 9:11–77Google Scholar
  17. Buddie AG, Bridge PD, Kelley J, Ryan MJ (2011) Candida keroseneae sp. nov., a novel contaminant of aviation kerosene. Lett Appl Microbiol 52(1):70–75PubMedCrossRefGoogle Scholar
  18. Cañero DC, Roncero MIG (2008) Functional analyses of laccase genes from Fusarium oxysporum. Phytopathology 98(5):509–518PubMedCrossRefGoogle Scholar
  19. Cerniglia CE, Sutherland JB (2010) In: Timmis KN (ed) Handbook of hydrocarbon and lipid microbiology. Springer, Berlin/Heidelberg, pp 2079–2110CrossRefGoogle Scholar
  20. Cerniglia CE, Sutherland JB, Crow SA (1992) In: Winkelmann G (ed) Microbial degradation of natural products. VCH Verlagsgesellschaft, Weinheim, pp 193–217Google Scholar
  21. Chen W, Lee M-K, Jefcoate C, Kim S-C, Chen F, Yu J-H (2014) Fungal cytochrome P450 monooxygenases: their distribution, structure, functions, family expansion, and evolutionary origin. Genome Biol Evol 6(7):1620–1634PubMedPubMedCentralCrossRefGoogle Scholar
  22. Chrzanowski Ł, Bielicka-Daszkiewicz K, Owsianiak M, Aurich A, Kaczorek E, Olszanowski A (2008) Phenol and n-alkanes (C12 and C16) utilization: influence on yeast cell surface hydrophobicity. World J Microbiol Biotechnol 24(9):1943–1949CrossRefGoogle Scholar
  23. Cofone L, Walker JD, Cooney JJ (1973) Utilization of hydrocarbons by Cladosporium resinae. Microbiology 76(1):243–246Google Scholar
  24. Cox HHJ, Houtman JHM, Doddema HJ, Harder W (1993a) Enrichment of fungi and degradation of styrene in biofilters. Biotechnol Lett 15(7):737–742CrossRefGoogle Scholar
  25. Cox HHJ, Houtman JHM, Doddema HJ, Harder W (1993b) Growth of the black yeast Exophiala jeanselmei on styrene and styrene-related compounds. Appl Microbiol Biotechnol 39(3):372–376CrossRefGoogle Scholar
  26. Cox HHJ, Faber BW, Van Heiningen WNM, Radhoe H, Doddema HJ, Harder W (1996) Styrene metabolism in Exophiala jeanselmei and involvement of a cytochrome P-450-dependent styrene monooxygenase. Appl Environ Microbiol 62(4):1471–1474PubMedPubMedCentralGoogle Scholar
  27. Curry S, Ciuffetti L, Hyman M (1996) Inhibition of growth of a Graphium sp. on gaseous n-alkanes by gaseous n-alkynes and n-alkenes. Appl Environ Microbiol 62(6):2198–2200PubMedPubMedCentralGoogle Scholar
  28. Dallinger A, Duldhardt I, Kabisch J, Schlüter R, Schauer F (2016) Biotransformation of cyclohexane and related alicyclic hydrocarbons by Candida maltosa and Trichosporon species. Int Biodeter Biodegr 107:132–139CrossRefGoogle Scholar
  29. David HM (1954) Studies of the creosote fungus, Hormodendrum resinae. Mycologia 46(2):161–183CrossRefGoogle Scholar
  30. Davies JS, Wellman AM, Zajic JE (1973) Hyphomycetes utilizing natural gas. Can J Microbiol 19(1):81–85PubMedCrossRefGoogle Scholar
  31. de Boer W, Folman LB, Summerbell RC, Boddy L (2005) Living in a fungal world: impact of fungi on soil bacterial niche development. FEMS Microbiol Rev 29(4):795–811PubMedCrossRefPubMedCentralGoogle Scholar
  32. de Hoog GS (1999) Ecology and evolution of black yeasts and their relatives. Stud Mycol 43:1–208Google Scholar
  33. de Hoog GS, Vicente VA, Caligiorne RB, Kantarcioglu S, Tintelnot K, Gerrits van den Ende AHG, Haase G (2003) Species diversity and polymorphism in the Exophiala spinifera clade containing opportunistic black yeast-like fungi. J Clin Microbiol 41(10):4767–4778PubMedPubMedCentralCrossRefGoogle Scholar
  34. Duarte APM, Attili-Angelis D, Baron NC, Forti LC, Pagnocca FC (2014) Leaf-cutting ants: an unexpected microenvironment holding human opportunistic black fungi. Antonie Van Leeuwenhoek 106(3):465–473PubMedCrossRefPubMedCentralGoogle Scholar
  35. Estevez E, Veiga MC, Kennes C (2005) Biodegradation of toluene by the new fungal isolates Paecilomyces variotii and Exophiala oligosperma. J Ind Microbiol Biotechnol 32(1):33–37PubMedCrossRefPubMedCentralGoogle Scholar
  36. Fedorak PM, Westlake DWS (1986) Fungal metabolism of n-alkylbenzenes. Appl Environ Microbiol 51(2):435–437PubMedPubMedCentralGoogle Scholar
  37. Fickers P, Benetti PH, Waché Y, Marty A, Mauersberger S, Smit MS, Nicaud JM (2005) Hydrophobic substrate utilisation by the yeast Yarrowia lipolytica, and its potential applications. FEMS Yeast Res 5(6–7):527–543PubMedCrossRefPubMedCentralGoogle Scholar
  38. Gadd GM (2001) Fungi in bioremediation. Cambridge University Press, CambridgeCrossRefGoogle Scholar
  39. García-Peña I, Ortiz I, Hernández S, Revah S (2008) Biofiltration of BTEX by the fungus Paecilomyces variotii. Int Biodeter Biodegr 62(4):442CrossRefGoogle Scholar
  40. Gassen J, Bento F, Frazzon A, Ferrão M, Marroni I, Simonetti A (2015) Growth of Paecilomyces variotii in B0 (diesel), B100 (biodiesel) and B7 (blend), degradation and molecular detection. Braz J Biol 75:541–547PubMedCrossRefGoogle Scholar
  41. Gaylarde CC, Bento FM, Kelley J (1999) Microbial contamination of stored hydrocarbon fuels and its control. Rev Microbiol 30(1):1–10CrossRefGoogle Scholar
  42. Ghosal D, Ghosh S, Dutta TK, Ahn Y (2016) Current state of knowledge in microbial degradation of polycyclic aromatic hydrocarbons (PAHs): a review. Front Microbiol 7:1369PubMedPubMedCentralGoogle Scholar
  43. Gibson DT, Subramanian V (1984) In: Gibson DT (ed) Microbial degradation of organic compounds. Marcel Dekker, New York, pp 181–252Google Scholar
  44. Gold MH, Alic M (1993) Molecular-biology of the lignin-degrading basidiomycete phanerochaete-chrysosporium. Microbiol Rev 57(3):605–622PubMedPubMedCentralGoogle Scholar
  45. Gries G, Smirle MJ, Leufven A, Miller DR, Borden JH, Whitney HS (1990) Conversion of phenylalanine to toluene and 2-phenylethanol by the pine engraver Ips-pini (Say) (Coleoptera, Scolytidae). Experientia 46(3):329–331CrossRefGoogle Scholar
  46. Gümral R, Tümgör A, Saraçlı MA, Yıldıran ŞT, Ilkit M, de Hoog GS (2014) Black yeast diversity on creosoted railway sleepers changes with ambient climatic conditions. Microb Ecol 68(4):699–707PubMedCrossRefPubMedCentralGoogle Scholar
  47. Gümral R, Özhak-Baysan B, Tümgör A, Saraçlı MA, Yıldıran ŞT, Ilkit M, Zupančič J, Novak-Babič M, Gunde-Cimerman N, Zalar P, de Hoog GS (2016) Dishwashers provide a selective extreme environment for human-opportunistic yeast-like fungi. Fungal Divers 76(1):1–9CrossRefGoogle Scholar
  48. Gutierrez JR, Erickson LE (1977) Hydrocarbon uptake in hydrocarbon fermentations. Biotechnol Bioeng 19(9):1331–1349PubMedCrossRefPubMedCentralGoogle Scholar
  49. Halecky M, Rousova J, Paca J, Kozliak E, Seames W, Jones K (2015) Biofiltration of gasoline and diesel aliphatic hydrocarbons. J Air Waste Manage Assoc 65(2):133–144CrossRefGoogle Scholar
  50. Haritash AK, Kaushik CP (2009) Biodegradation aspects of polycyclic aromatic hydrocarbons (PAHs): a review. J Hazard Mater 169(1):1–15PubMedCrossRefPubMedCentralGoogle Scholar
  51. Harms H, Schlosser D, Wick LY (2011) Untapped potential: exploiting fungi in bioremediation of hazardous chemicals. Nat Rev Microbiol 9(3):177–192PubMedCrossRefGoogle Scholar
  52. Hasegawa Y, Yoshioka N, Obata H, Kawate S, Yoshizako F, Kaneda T, Tokuyama T (1990) Degradation of cyclohexanone by Exophiala jeanselmei. Nippon Nogeikagaku Kaishi 64(2):157–162CrossRefGoogle Scholar
  53. Heider J, Schühle K (2013) In: Rosenberg E, DeLong EF, Lory S, Stackebrandt E, Thompson F (eds) The prokaryotes: prokaryotic physiology and biochemistry. Springer, Berlin/Heidelberg, pp 605–634CrossRefGoogle Scholar
  54. Hofrichter M (2002) Review: lignin conversion by manganese peroxidase (MnP). Enzym Microb Technol 30(4):454–466CrossRefGoogle Scholar
  55. Hölker U, Bend J, Pracht R, Tetsch L, Muller T, Hofer M, de Hoog GS (2004) Hortaea acidophila, a new acid-tolerant black yeast from lignite. Antonie Van Leeuwenhoek 86(4):287–294PubMedCrossRefGoogle Scholar
  56. Hug H, Fiechter A (1972) Assimilation of aliphatic hydrocarbons by Candida tropicalis. Arch Mikrobiol 88(2):77–86CrossRefGoogle Scholar
  57. Ishijima SA, Yamada T, Maruyama N, Abe S (2017) Candida albicans adheres to chitin by recognizing N-acetylglucosamine (GlcNAc). Med Mycol J 58(1):E15–E21PubMedCrossRefGoogle Scholar
  58. Isola D, Selbmann L, Hoog GS, Fenice M, Onofri S, Prenafeta-Boldú F, Zucconi L (2013) Isolation and screening of black fungi as degraders of volatile aromatic hydrocarbons. Mycopathologia 175(5–6):369–379PubMedCrossRefGoogle Scholar
  59. Isola D, Zucconi L, Onofri S, Caneva G, de Hoog GS, Selbmann L (2016) Extremotolerant rock inhabiting black fungi from Italian monumental sites. Fungal Divers 76(1):75–96CrossRefGoogle Scholar
  60. Janda-Ulfig K, Ulfig K, Cano J, Guarro J (2008) A study of the growth of Pseudallescheria boydii isolates from sewage sludge and clinical sources on tributyrin, rapeseed oil, biodiesel oil and diesel. Ann Agric Environ Med 15(1):45–49PubMedPubMedCentralGoogle Scholar
  61. Jin Y, Veiga MC, Kennes C (2006) Performance optimization of the fungal biodegradation of α-pinene in gas-phase biofilter. Process Biochem 41(8):1722CrossRefGoogle Scholar
  62. Juhasz AL, Naidu R (2000) Bioremediation of high molecular weight polycyclic aromatic hydrocarbons: a review of the microbial degradation of benzo[a]pyrene. Int Biodeter Biodegr 45(1):57–88CrossRefGoogle Scholar
  63. Kadri T, Rouissi T, Kaur Brar S, Cledon M, Sarma S, Verma M (2017) Biodegradation of polycyclic aromatic hydrocarbons (PAHs) by fungal enzymes: a review. J Environ Sci 51:52–74CrossRefGoogle Scholar
  64. Kaltseis J, Rainer J, De Hoog GS, Kaltseis J, Rainer J, De Hoog GS (2009) Ecology of Pseudallescheria and Scedosporium species in human-dominated and natural environments and their distribution in clinical samples. Med Mycol 47(4):398–405PubMedCrossRefGoogle Scholar
  65. Kennes C, Veiga MC (2004) Fungal biocatalysts in the biofiltration of VOC-polluted air. J Biotechnol 113(1–3):305–319PubMedCrossRefGoogle Scholar
  66. Kennes C, Veiga MC (2012) In: Singh SN (ed) Microbial degradation of xenobiotics. Springer, Berlin/Heidelberg, pp 177–188CrossRefGoogle Scholar
  67. Klepzig KD, Six DL (2004) Bark beetle-fungal symbiosis: context dependency in complex associations. Symbiosis 37(1–3):189–205Google Scholar
  68. Kobayashi T, Murai Y, Tatsumi K, Iimura Y (2009) Biodegradation of polycyclic aromatic hydrocarbons by Sphingomonas sp. enhanced by water-extractable organic matter from manure compost. Sci Total Environ 407(22):5805–5810PubMedCrossRefGoogle Scholar
  69. Kohlmeier S, Smits THM, Ford RM, Keel C, Harms H, Wick LY (2005) Taking the fungal highway: mobilization of pollutant-degrading bacteria by fungi. Environ Sci Technol 39(12):4640–4646PubMedCrossRefGoogle Scholar
  70. Kremer S, Anke H (1997) In: Anke T (ed) Fungal biotechnology. Chapman & Hall, Weinheim, pp 275–295Google Scholar
  71. Lamb DC, Lei L, Warrilow AGS, Lepesheva GI, Mullins JGL, Waterman MR, Kelly SL (2009) The first virally encoded cytochrome P450. J Virol 83(16):8266–8269PubMedPubMedCentralCrossRefGoogle Scholar
  72. Lebrero R, López JC, Lehtinen I, Pérez R, Quijano G, Muñoz R (2016) Exploring the potential of fungi for methane abatement: performance evaluation of a fungal-bacterial biofilter. Chemosphere 144:97–106PubMedCrossRefGoogle Scholar
  73. Leelaruji W, Buathong P, Kanngan P, Piamtongkam R, Chulalaksananukul S, Wattayakorn G, Chulalaksananukul W (2014) Potential of laccase produced from microfungus, Aureobasidium pullulans var. melanogenum, to degrade poly-aromatic hydrocarbons. Eur Chem Bull 3(3):269–272Google Scholar
  74. Lindley ND (1992) In: Arora DK, Elander RP, Mukerji KG (eds) Handbook of applied mycology. Marcel Dekker, New York, pp 905–929Google Scholar
  75. Lindley ND, Heydeman MT (1983) Uptake of vapour phase [14C]dodecane by whole mycelia of Cladosporium resinae. Microbiology 129(7):2301–2305CrossRefGoogle Scholar
  76. Little B, Ray R (2001) A review of fungal influenced corrosion. Corros Rev 19(5–6):401Google Scholar
  77. Luykx DMA, Prenafeta-Boldú FX, de Bont JAM (2003) Toluene monooxygenase from the fungus Cladosporium sphaerospermum. Biochem Biophys Res Commun 312:373–379PubMedCrossRefGoogle Scholar
  78. Majcherczyk A, Johannes C, Hüttermann A (1998) Oxidation of polycyclic aromatic hydrocarbons (PAH) by laccase of Trametes versicolor. Enzym Microb Technol 22(5):335–341CrossRefGoogle Scholar
  79. Marco-Urrea E, García-Romera I, Aranda E (2015) Potential of non-ligninolytic fungi in bioremediation of chlorinated and polycyclic aromatic hydrocarbons. New Biotechnol 32(6):620–628CrossRefGoogle Scholar
  80. Martin-Sanchez PM, Nováková¡ A, Bastian F, Alabouvette C, Saiz-Jimenez C (2012) Use of biocides for the control of fungal outbreaks in subterranean environments: the case of the Lascaux Cave in France. Environ Sci Technol 46(7):3762–3770PubMedCrossRefGoogle Scholar
  81. Martin-Sanchez PM, Gorbushina AA, Kunte H-J, Toepel J (2016a) A novel qPCR protocol for the specific detection and quantification of the fuel-deteriorating fungus Hormoconis resinae. Biofouling 32(6):635–644PubMedCrossRefGoogle Scholar
  82. Martin-Sanchez PM, Gorbushina AA, Toepel J (2016b) Quantification of microbial load in diesel storage tanks using culture- and qPCR-based approaches. Int Biodeter Biodegr 126:216–223CrossRefGoogle Scholar
  83. Mayer AM, Staples RC (2002) Laccase: new functions for an old enzyme. Phytochemistry 60(6):551–565PubMedCrossRefGoogle Scholar
  84. Middelhoven WJ (2006) Polysaccharides and phenolic compounds as substrate for yeasts isolated from rotten wood and description of Cryptococcus fagi sp.nov. Antonie Van Leeuwenhoek 90(1):57–67PubMedCrossRefGoogle Scholar
  85. Middelhoven WJ, Kurtzman CP (2007) Four novel yeasts from decaying organic matter: Blastobotrys robertii sp. nov., Candida cretensis sp. nov., Candida scorzettiae sp. nov. and Candida vadensis sp. nov. Antonie Van Leeuwenhoek 92(2):233–244PubMedCrossRefGoogle Scholar
  86. Middelhoven WJ, Scorzetti G, Fell JW (1999) Trichosporon guehoae sp.nov., an anamorphic basidiomycetous yeast. Can J Microbiol 45(8):686–690PubMedCrossRefGoogle Scholar
  87. Middelhoven WJ, Scorzetti G, Fell JW (2000) Trichosporon veenhuisii sp. nov., an alkane-assimilating anamorphic basidiomycetous yeast. Int J Syst Evol Microbiol 50(1):381–387PubMedCrossRefGoogle Scholar
  88. Middelhoven WJ, Fonseca A, Carreiro SC, Carlos Pagnocca F, Bueno OC (2003) Cryptococcus haglerorum, sp. nov., an anamorphic basidiomycetous yeast isolated from nests of the leaf-cutting ant Atta sexdens. Antonie Van Leeuwenhoek 83(2):167–174PubMedCrossRefGoogle Scholar
  89. Moreno LF, Feng P, Weiss VA, Vicente VA, Stielow JB, de Hoog S (2017) Phylogenomic analyses reveal the diversity of laccase-coding genes in Fonsecaea genomes. PLoS One 12(2):e0171291PubMedPubMedCentralCrossRefGoogle Scholar
  90. Moreno LF, Ahmed AAO, Brankovics B, Cuomo CA, Menken SBJ, Taj-Aldeen SJ, Faidah H, Stielow JB, de M Teixeira M, Prenafeta-Boldú FX, Vicente VA, de Hoog S (2018) Genomic understanding of an infectious brain disease from the desert. G3 (in press), 8, 300421Google Scholar
  91. Mulheirn L, Van Eyk J (1981) Microbiological oxidation of steroid hydrocarbons. Microbiology 126(2):267–275CrossRefGoogle Scholar
  92. Muncnerova D, Augustin J (1994) Fungal metabolism and detoxification of polycyclic aromatic hydrocarbons: a review. Bioresour Technol 48(2):97–106CrossRefGoogle Scholar
  93. Napolitano R, Juárez MP (1997) Entomopathogenous fungi degrade epicuticular hydrocarbons of Triatoma infestans. Arch Biochem Biophys 344(1):208–214PubMedCrossRefGoogle Scholar
  94. Naranjo L, Pernía B, Inojosa Y, Rojas D, D’Anna LS, González M, Sisto ÁD (2015) First evidence of fungal strains isolated and identified from naphtha storage tanks and transporting pipelines in Venezuelan oil facilities. Adv Microbiol 05(02):12CrossRefGoogle Scholar
  95. Nascimento MMF, Vicente VA, Bittencourt JVM, Gelinski JML, Prenafeta-Boldú FX, Romero-Güiza M, Fornari G, Gomes RR, Santos GD, Gerrits Van Den Ende AHG, de Azevedo CDMPS, De Hoog GS (2017) Diversity of opportunistic black fungi on babassu coconut shells, a rich source of esters and hydrocarbons. Fungal Biol 121(5):488–500PubMedCrossRefGoogle Scholar
  96. Onodera M, Sakai H, Endo Y, Ogasawara N (1990) Oxidation of short-chain isoalkanes by gaseous hydrocarbon assimilating mold, Scedosporium sp. A-4. Agric Biol Chem 53(7):1947–1989Google Scholar
  97. Osono T (2007) Ecology of ligninolytic fungi associated with leaf litter decomposition. Ecol Res 22(6):955–974CrossRefGoogle Scholar
  98. Parbery D (1971) Biological problems in jet aviation fuel and the biology of Amorphotheca resinae. Mater Org 6:161–208Google Scholar
  99. Passman FJ (2013) Microbial contamination and its control in fuels and fuel systems since 1980 – a review. Int Biodeter Biodegr 81:88–104CrossRefGoogle Scholar
  100. Potin O, Veignie E, Rafin C (2004) Biodegradation of polycyclic aromatic hydrocarbons (PAHs) by Cladosporium sphaerospermum isolated from an aged PAH contaminated soil. FEMS Microbiol Ecol 51(1):71–78PubMedCrossRefGoogle Scholar
  101. Pozdnyakova NN (2012) Involvement of the ligninolytic system of white-rot and litter-decomposing fungi in the degradation of polycyclic aromatic hydrocarbons. Biotechnol Res Int 2012:20CrossRefGoogle Scholar
  102. Prenafeta-Boldú FX, Kuhn A, Luykx D, Anke H, van Groenestijn JW, de Bont JAM (2001a) Isolation and characterisation of fungi growing on volatile aromatic hydrocarbons as their sole carbon and energy source. Mycol Res 105(4):477–484CrossRefGoogle Scholar
  103. Prenafeta-Boldú FX, Luykx DMA, Vervoort J, de Bont JAM (2001b) Fungal metabolism of toluene: monitoring of fluorinated analogs by 19F nuclear magnetic resonance spectroscopy. Appl Environ Microbiol 67(3):1030–1034PubMedPubMedCentralCrossRefGoogle Scholar
  104. Prenafeta-Boldú FX, Vervoort J, Grotenhuis JTC, van Groenestijn JW (2002) Substrate interactions during the biodegradation of benzene, toluene, ethylbenzene, and xylene (BTEX) hydrocarbons by the fungus Cladophialophora sp. strain T1. Appl Environ Microbiol 68(6):2660–2665PubMedPubMedCentralCrossRefGoogle Scholar
  105. Prenafeta-Boldú FX, Summerbell R, de Hoog GS (2006) Fungi growing on aromatic hydrocarbons: biotechnology’s unexpected encounter with biohazard? FEMS Microbiol Rev 30:109–130PubMedCrossRefGoogle Scholar
  106. Prenafeta-Boldú FX, Guivernau M, Gallastegui G, Viñas M, de Hoog GS, Elías A (2012) Fungal/bacterial interactions during the biodegradation of TEX hydrocarbons (toluene, ethylbenzene and p-xylene) in gas biofilters operated under xerophilic conditions. FEMS Microbiol Ecol 80(3):722–734PubMedCrossRefGoogle Scholar
  107. Prince RC (2010) In: Timmis KN (ed) Handbook of hydrocarbon and lipid microbiology. Springer, Berlin/Heidelberg, pp 2065–2078CrossRefGoogle Scholar
  108. Purchase D (2016) Fungal applications in sustainable environmental biotechnology. Springer, ChamGoogle Scholar
  109. Qi B, Moe W, Kinney K (2002) Biodegradation of volatile organic compounds by five fungal species. Appl Microbiol Biotechnol 58(5):684–689PubMedCrossRefGoogle Scholar
  110. Qi B, Moe WM, Kinney KA (2005) Treatment of paint spray booth off-gases in a fungal biofilter. J Environ Eng ASCE 131(2):180–189CrossRefGoogle Scholar
  111. Rafin C, Potin O, Veignie E, Sancholle M (2000) Degradation of benzo[a]pyrene as sole carbon source by a non white rot fungus, Fusarium solani. Polycycl Aromat Compd 21(1):311–329Google Scholar
  112. Rafin C, Veignie E, Woisel P, Cazier F, Surpateanu G (2008) Modern multidisciplinary applied microbiology. Wiley-VCH, Weinheim, pp 546–550Google Scholar
  113. Raj HG, Saxena M, Allameh A (1992) In: Arora DK, Elander RP, Mukerji KG (eds) Handbook of applied mycology. Marcel Dekker, New York, pp 881–904Google Scholar
  114. Ralebitso-Senior TK, Senior E, Di Felice R, Jarvis K (2012) Waste gas biofiltration: advances and limitations of current approaches in microbiology. Environ Sci Technol 46(16):8542–8573PubMedCrossRefGoogle Scholar
  115. Reddy CA, D’Souza TM (1994) Physiology and molecular biology of the lignin peroxidases of Phanerochaete chrysosporium. FEMS Microbiol Rev 13:137–152PubMedCrossRefGoogle Scholar
  116. Rehm HJ, Reiff J (1981) In: Fiechter A (ed) Advances in biochemical engineering. Springer, Berlin, pp 175–215Google Scholar
  117. Rene ER, Veiga MC, Kennes C (2010) Biodegradation of gas-phase styrene using the fungus Sporothrix variecibatus: impact of pollutant load and transient operation. Chemosphere 79(2):221–227PubMedCrossRefGoogle Scholar
  118. Restrepo-Flórez J-M, Bassi A, Thompson MR (2014) Microbial degradation and deterioration of polyethylene – a review. Int Biodeter Biodegr 88:83–90CrossRefGoogle Scholar
  119. Restrepo-Flórez J-M, Wood JA, Rehmann L, Thompson M, Bassi A (2015) Effect of biodiesel on biofilm biodeterioration of linear low density polyethylene in a simulated fuel storage tank. J Energy Resour Technol 137(3):032211-032211-032216CrossRefGoogle Scholar
  120. Reyes-César A, Absalón ÁE, Fernández FJ, González JM, Cortés-Espinosa DV (2014) Biodegradation of a mixture of PAHs by non-ligninolytic fungal strains isolated from crude oil-contaminated soil. World J Microbiol Biotechnol 30(3):999–1009PubMedCrossRefGoogle Scholar
  121. Rodriguez A, Perestelo F, Carnicero A, Regalado V, Perez R, De la Fuente G, Falcon MA (1996) Degradation of natural lignins and lignocellulosic substrates by soil-inhabiting fungi imperfecti. FEMS Microbiol Ecol 21(3):213–219CrossRefGoogle Scholar
  122. Rodríguez-Rodríguez CE, Rodríguez E, Blanco R, Cordero I, Segura D (2010) Fungal contamination of stored automobile-fuels in a tropical environment. J Environ Sci 22(10):1595–1601CrossRefGoogle Scholar
  123. Rosenberg E (2013) In: Rosenberg E, DeLong EF, Lory S, Stackebrandt E, Thompson F (eds) The prokaryotes: prokaryotic physiology and biochemistry. Springer, Berlin/Heidelberg, pp 201–214CrossRefGoogle Scholar
  124. Ruiz-Dueñas FJ, Morales M, García E, Miki Y, Martínez MJ, Martínez AT (2009) Substrate oxidation sites in versatile peroxidase and other basidiomycete peroxidases. J Exp Bot 60(2):441–452PubMedCrossRefGoogle Scholar
  125. Saparrat MCN, Martínez MJ, Tournier HA, Cabello MN, Arambarri AM (2000) Production of ligninolytic enzymes by Fusarium solani strains isolated from different substrata. World J Microbiol Biotechnol 16(8):799–803CrossRefGoogle Scholar
  126. Sariaslani FS (1991) Microbial cytochromes P-450 and xenobiotic metabolism. Adv Appl Microbiol 36:133–178PubMedCrossRefGoogle Scholar
  127. Satow MM, Attili-Angelis D, de Hoog GS, Angelis DF, Vicente VA (2008) Selective factors involved in oil flotation isolation of black yeasts from the environment. Stud Mycol 61(1):157–163PubMedPubMedCentralCrossRefGoogle Scholar
  128. Sikkema J, de Bont J, Poolman B (1995) Mechanisms of membrane toxicity of hydrocarbons. Microbiol Rev 59(2):201–222PubMedPubMedCentralGoogle Scholar
  129. Singleton I (2001) In: Gadd G (ed) Fungi in bioremediation. Cambridge University Press, Cambridge, pp 79–96CrossRefGoogle Scholar
  130. Soriano AU, Martins LF, Santos de Assumpção Ventura E, Teixeira Gerken de Landa FH, de Araújo Valoni É, Dutra Faria FR, Ferreira RF, Kremer Faller MC, Valério RR, Catharine de Assis Leite D, Lima do Carmo F, Peixoto RS (2015) Microbiological aspects of biodiesel and biodiesel/diesel blends biodeterioration. Int Biodeter Biodegr 99:102–114CrossRefGoogle Scholar
  131. Sorkhoh NA, Ghannoum MA, Ibrahim AS, Stretton RJ, Radwan SS (1990) Growth of Candida albicans on hydrocarbons: influence on lipids and sterols. Microbios 64:260–261Google Scholar
  132. Spigno G, Pagella C, Fumi MD, Molteni R, de Faveri DM (2003) VOCs removal from waste gases: gas-phase bioreactor for the abatement of hexane by Aspergillus niger. Chem Eng Sci 58(3–6):739–746CrossRefGoogle Scholar
  133. Sprenger B, Rehm HJ (1983) Biomass production by Candida species from n-alkanes in a film-submerged reactor in comparison with known culture methods. Eur J Appl Microbiol Biotechnol 17(1):64–68CrossRefGoogle Scholar
  134. Steffen KT, Schubert S, Tuomela M, Hatakka A, Hofrichter M (2007) Enhancement of bioconversion of high-molecular mass polycyclic aromatic hydrocarbons in contaminated non-sterile soil by litter-decomposing fungi. Biodegradation 18(3):359–369PubMedCrossRefGoogle Scholar
  135. Sutherland J (2003) Fungal biotechnology in agricultural, food, and environmental applications. CRC Press, New York, pp 443–456Google Scholar
  136. Syed K, Porollo A, Lam YW, Grimmett PE, Yadav JS (2013) CYP63A2, a catalytically versatile fungal P450 monooxygenase capable of oxidizing higher-molecular-weight polycyclic aromatic hydrocarbons, alkylphenols, and alkanes. Appl Environ Microbiol 79(8):2692–2702PubMedPubMedCentralCrossRefGoogle Scholar
  137. Teixeira MM, Moreno LF, Stielow BJ, Muszewska A, Hainaut M, Gonzaga L, Abouelleil A, Patané JSL, Priest M, Souza R, Young S, Ferreira KS, Zeng Q, da Cunha MML, Gladki A, Barker B, Vicente VA, de Souza EM, Almeida S, Henrissat B, Vasconcelos ATR, Deng S, Voglmayr H, Moussa TAA, Gorbushina A, Felipe MSS, Cuomo CA, de Hoog GS (2017) Exploring the genomic diversity of black yeasts and relatives (Chaetothyriales, Ascomycota). Stud Mycol 86:1–28PubMedPubMedCentralCrossRefGoogle Scholar
  138. Tetsch L, Bend J, Hölker U (2006) Molecular and enzymatic characterisation of extra- and intracellular laccases from the acidophilic ascomycete Hortaea acidophila. Antonie Van Leeuwenhoek 90(2):183–194PubMedCrossRefGoogle Scholar
  139. Toledo AV, Virla E, Humber RA, Paradell SL, Lastra CCL (2006) First record of Clonostachys rosea (Ascomycota: Hypocreales) as an entomopathogenic fungus of Oncometopia tucumana and Sonesimia grossa (Hemiptera: Cicadellidae) in Argentina. J Invertebr Pathol 92(1):7–10PubMedCrossRefGoogle Scholar
  140. Tomaselli Scotti C, Durand A (2000) Soil bioremediation by a fungal inoculum of Cunninghamella elegans produced by solid state cultivation. Agro Food Ind Hi Tech 11(4):37–40Google Scholar
  141. Trippe KM, Wolpert TJ, Hyman MR, Ciuffetti LM (2014) RNAi silencing of a cytochrome P450 monoxygenase disrupts the ability of a filamentous fungus, Graphium sp., to grow on short-chain gaseous alkanes and ethers. Biodegradation 25(1):137–151PubMedCrossRefPubMedCentralGoogle Scholar
  142. van den Brink HJM, van Gorcom RFM, van den Hondel CAMJJ, Punt PJ (1998) Cytochrome P450 enzyme systems in fungi. Fungal Genet Biol 23(1):1–17PubMedCrossRefGoogle Scholar
  143. van Groenestijn JW, Liu JX (2002) Removal of alpha-pinene from gases using biofilters containing fungi. Atmos Environ 36(35):5501–5508CrossRefGoogle Scholar
  144. van Groenestijn JW, van Heiningen WNM, Kraakman NJR (2001) Biofilters based on the action of fungi. Water Sci Technol 44(9):227–232PubMedCrossRefGoogle Scholar
  145. Vigueras G, Shirai K, Hernández-Guerrero M, Morales M, Revah S (2014) Growth of the fungus Paecilomyces lilacinus with n-hexadecane in submerged and solid-state cultures and recovery of hydrophobin proteins. Process Biochem 49(10):1606–1611CrossRefGoogle Scholar
  146. Voglmayr H, Mayer V, Maschwitz U, Moog J, Djieto-Lordon C, Blatrix R (2011) The diversity of ant-associated black yeasts: insights into a newly discovered world of symbiotic interactions. Fungal Biol 115(10):1077–1091PubMedCrossRefGoogle Scholar
  147. Wainwright M (1993) In: Jennings DH (ed) Stress tolerance of fungi. Marcel Dekker, New York, pp 127–144Google Scholar
  148. Wang W-J, Wang X-L, Li Y, Xiao S-R, Kepler RM, Yao Y-J (2012) Molecular and morphological studies of Paecilomyces sinensis reveal a new clade in clavicipitaceous fungi and its new systematic position. Syst Biodivers 10(2):221–232CrossRefGoogle Scholar
  149. Weber FJ, Hage KC, de Bont JAM (1995) Growth of the fungus Cladosporium sphaerospermum with toluene as the sole carbon and energy source. Appl Environ Microbiol 61(10):3562–3566PubMedPubMedCentralGoogle Scholar
  150. Winquist E, Björklöf K, Schultz E, Räsänen M, Salonen K, Anasonye F, Cajthaml T, Steffen KT, Jørgensen KS, Tuomela M (2014) Bioremediation of PAH-contaminated soil with fungi – from laboratory to field scale. Int Biodeter Biodegr 86(Part C):238–247CrossRefGoogle Scholar
  151. Woertz JR, Kinney KA, McIntosh NDP (2001) Removal of toluene in a vapor-phase bioreactor containing a strain of the dimorphic black yeast Exophiala lecanii-corni. Biotechnol Bioeng 75:550–558PubMedCrossRefGoogle Scholar
  152. Wolf HJ, Hanson RS (1980) Identification of methane-utilizing yeasts. FEMS Microbiol Lett 7(2):177–179CrossRefGoogle Scholar
  153. Wu Y-R, Luo Z-H, Kwok-Kei Chow R, Vrijmoed LLP (2010) Purification and characterization of an extracellular laccase from the anthracene-degrading fungus Fusarium solani MAS2. Bioresour Technol 101(24):9772–9777PubMedCrossRefPubMedCentralGoogle Scholar
  154. Yadav JS, Reddy CA (1993) Degradation of benzene, toluene, ethylbenzene and xylenes (BTEX) by the lignin-degrading basidiomycete Phanerochaete chrysosporium. Appl Environ Microbiol 59(3):756–762PubMedPubMedCentralGoogle Scholar
  155. Yemashova NA, Murygina VP, Zhukov DV, Zakharyantz AA, Gladchenko MA, Appanna V, Kalyuzhnyi SV (2007) Biodeterioration of crude oil and oil derived products: a review. Rev Environ Sci Biotechnol 6(4):315–337CrossRefGoogle Scholar
  156. Zhang D, Yang Y, Leakey JEA, Cerniglia CE (1996) Phase I and phase II enzymes produced by Cunninghamella elegans for the metabolism of xenobiotics. FEMS Microbiol Lett 138(2–3):221–226PubMedCrossRefPubMedCentralGoogle Scholar
  157. Zhao J, Zeng J, de Hoog G, Attili-Angelis D, Prenafeta-Boldú F (2010) Isolation and identification of black yeasts by enrichment on atmospheres of monoaromatic hydrocarbons. Microb Ecol 60(1):149–156PubMedPubMedCentralCrossRefGoogle Scholar
  158. ZoBell CE (1946) Action of microorganisms on hydrocarbons. Bacteriol Rev 10:1–49PubMedPubMedCentralGoogle Scholar

Copyright information

© Springer Nature Switzerland AG 2019

Authors and Affiliations

  • Francesc X. Prenafeta-Boldú
    • 1
    Email author
  • G. Sybren de Hoog
    • 2
    • 3
  • Richard C. Summerbell
    • 4
    • 5
  1. 1.Integral Management of Organic Waste (GIRO)Institute of Agrifood Research and Technology (IRTA)Caldes de MontbuiSpain
  2. 2.Westerdijk Fungal Biodiversity InstituteUtrechtThe Netherlands
  3. 3.Center of Expertise in Mycology of RadboudUMC / Canisius Wilhelmina HospitalRadboud UniversityNijmegenThe Netherlands
  4. 4.Sporometrics IncTorontoCanada
  5. 5.University of Toronto, Dalla Lana School of Public HealthTorontoCanada

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